Metal composition of zooplankton from
the Western Indian Ocean
JD van Aswegen
orcid.org 0000-0001-8482-6974
Dissertation accepted in fulfilment of the requirements for the
degree
Master of Science in Environmental Sciences
at the
North-West University
Supervisor: Prof H Bouwman
i
Acknowledgements
• I would like to thank my supervision Prof. H Bouwman, for the mentorship he provided me with over these years. Thank you for taking a chance and believing in me.
• I would like to thank the POPT group for using their facilities.
• I would especially like to thank everyone from the IIOE II for fantastic adventures and forever memories.
• I would like to thank all my friends; without you, I would have surely lost my marbles long ago.
• To my family, these years were trying for us as a family. Thank you for your love and for supporting me fully in my endeavours no matter how ambitious.
Abstract
The Indian Ocean is probably the least researched ocean of the world. It is the third largest ocean and has many unique topographic, geologic, oceanographic, biological, and socio-economic features. The current system is also complex and variable on small and large scales. Uniquely, there is a component of monsoon seasonality affecting currents.
In terms of zooplankton, little is known, and even less is published on metals, a major component of a class of pollutants that also occurs naturally. Due to development, trade, shipping (especially oil), an expanding human population, coupled with current and potential conflict, knowledge on the current state of pollution (or lack of) is needed to tract future impacts and development.
Plankton is one of the most important components of the ecology of any ocean. Pollutants can affect plankton, change the characteristics of pollutants, and can be assimilated and/or bioconcentrated. They also play major roles in the carbon and nitrogen cycles and the microbial loop. Disturbances of these major processes may affect ecosystem functions and affect human communities depending of the ocean. Metals, although all occurring naturally in seawater, may be elevated beyond natural background levels due to pollution, posing risk to biota.
Although some ecotoxicological work has been done on mammals, fish, birds, and coral, there is a great lack of knowledge regarding metal composition in zooplankton from the western Indian Ocean (WIO), the region where I conducted my research. In this region, I concentrated on the metal compositions of three currents. The South Equatorial Current (SEC) is the main current that carries warm water from the east towards the African continent. This current runs through the tropical region of the Indian Ocean where it branches into the Madagascar Current (MC) flowing south, and East African Coastal Current (EACC). Each of these currents have upwellings and eddies. The two latter currents also receive freshwater discharges (containing metals) from many rivers along the coast, while volcanic activity in the SEC might contribute metals as well.
I collected 94 zooplankton samples from the three currents, and analysed them with ICP-MS for 34 metallic elements. I analysed the data statistically but also looked at geographic interpolation.
Although I analysed 34 elements, I concentrated on 14 essential (V, Cr, Mn, Fe, Co, Cu, Zn, As, and Se) and five non-essential (Ni, Cd, Hg, Pb, and U) elements as set out by the ATSDR’s substance priority list, and compared the elemental distributions and concentrations in zooplankton from the three currents. There were differences in concentrations of some elements between the three currents – each current therefore had distinguishable but subtle compositions of metals in their zooplankton. For many of
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I found that V, Cr, As, Se, Hg, Ni, and U concentrations in zooplankton from some sites approached and exceeded the concentrations found in other studies. To the best of our knowledge, Ni had the second highest recorded concentration. With high concentrations from “hot spots”, a certain amount of concern is warranted. Geographically, a number of “hot spots” were found, mainly associated with harbours and river mouths of the MC and EACC, and some in shallow areas near the African mainland. However, there were differences in concentrations between these “hot spots”. There were also indications of volcanic contributions of metals in zooplankton collected from the SEC.
I cannot conclude definitively that increased concentrations of metals in zooplankton from the EACC, MC, and SEC “hot spots” were solely from terrestrial sources or linked with pollution. The “hot spots” do suggest localised impacts that were not natural, apart from volcanic activity. Factors such as currents, upwelling, atmospheric deposition and primary productivity can affect the concentrations of metals in zooplankton. Currents close to the coast, eddies, and seasonal effects can influence the stratification (mixing) of nutrients, zooplankton, and metals in the water column, and therefore concentrations in zooplankton.
I therefore recommend further research into phytoplankton and zooplankton from the WIO as well as research into water and sediment concentrations, especially near “hot spots”, as this will more closely identify different sources of metals and indicate areas to reduce metal pollution.
My research has established a baseline against which future studies can measure changes linked to pollution, and identified certain metals and locations that would warrant closer attention
Key words: Zooplankton, Western Indian Ocean, Metals, Mozambique Channel, East African Coastal Current, South Equatorial Current
Table of Content
ACKNOWLEDGEMENTS ... I
ABSTRACT ... II
CHAPTER 1: INTRODUCTION ... 1
1.1. General introduction ... 1
1.2. The Indian Ocean ... 4
1.2.1. Indian Ocean topography ... 4
1.2.2. Indian Ocean currents ... 5
1.2.3. The Mozambique Channel (MC) ... 7
1.2.4. Eddies ... 8
1.2.5. Upwellings ... 9
1.2.6. Ocean zonation ... 10
1.3. Biogeochemical cycles ... 11
1.3.1. The carbon cycle ... 11
1.3.2. The nitrogen cycle ... 11
1.3.3. The microbial loop ... 12
1.4. Trace metals in the Marine Environment ... 12
1.4.1. Metabolic and physiological influences of metals ... 13
1.4.2. Oceanic nutrient transport ... 14
1.4.3. River runoff ... 15
1.5. Role of plankton ... 15
1.5.1. History of zooplankton research in the Indian Ocean ... 16
1.5.2. Trace metals in Zooplankton ... 17
1.6 Aim and objectives ... 18
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2.2.1. Mozambique Channel: MC (Mozambique) ... 21
2.2.2. East African Coastal Current: EACC (Tanzania) ... 23
2.2.3. South Equatorial Current: SEC (Comoros) ... 25
2.3. Sample collection and preparation ... 26
2.4. Laboratory analysis ... 28
2.5. Statistical analysis ... 29
CHAPTER 3: RESULTS ... 30
3.1. Analytical data ... 30
3.2. Physical and chemical analysis ... 40
3.3. Calcium-based comparisons ... 44
3.4. Multivariate analysis ... 51
3.5. Elemental comparative studies ... 53
3.6. Geographical distributions ... 55 3.6.1. Vanadium ... 55 3.6.2. Chromium ... 57 3.6.3. Manganese ... 58 3.6.4. Iron ... 60 3.6.5. Cobalt ... 61 3.6.6. Copper ... 63 3.6.7. Zinc ... 64 3.6.8. Arsenic ... 66 3.6.9. Selenium ... 67 3.6.10. Nickel ... 69 3.6.11. Cadmium ... 70 3.6.12. Mercury ... 71 3.6.13. Lead ... 73 3.6.14. Uranium ... 74
CHAPTER 4: DISCUSSION AND CONCLUSION ... 78
Elemental comparative studies with possible toxicological effects ... 78
4.1. Essential elements ... 78
4.2. Non-essential elements ... 80
Chapter 1: Introduction
1.1. General introduction
With a growing human population associated with increased urbanization and industrialization, a negative impact on a series of environments can be seen (Tu et al., 2014). Environmental changes are happening at an unprecedented rate and occur at regional and global scales, influencing terrestrial and aquatic organisms (Hood et al., 2015; Tu et al., 2014). Today’s environment is troubled by many problems, but the most threatening problem, arguably, remains combined stressors interacting with fresh- and marine waters.
The earth surface consists of 71% water, of which the marine environment makes up 96.5%. Approximately only 5% of marine species and effects of stress have been studied (Nunez, 2019). The marine and estuarine environments experience many forms and magnitudes of environmental stressors. These stressors push the boundaries of a normal environment due to the variation and differences caused by anthropogenic activities. The high frequency and intensity of these stressors tends to influence organisms, populations, and communities (Hood et al., 2015).
Environmental stressors that have the biggest impact on the Indian Ocean includes rise in sea temperature, rise in sea-levels, ocean acidification (increased CO2), eutrophication (increased N
and P), deoxygenation, plastic, and metal pollution (Hood et al., 2015; Obura et al., 2019). These specific stressors have unforeseen circumstances on the coastal marine environment and are influencing the general biogeochemical cycles of oceans, including the Indian Ocean, the area of my study. In some cases, the intensity and impact of human activities is unprecedented and could eventually pose a threat to human food security. Current trends suggest if these activities are not managed and mitigated, they are likely to increase with a concomitant increase in threats to the environment. An additional concern is that these activities are continuously increasing, affecting the world’s oceans, including the Indian Ocean (Hood et al., 2015; Obura et al., 2019).
Coastal ecosystems are of great interest where many complex physical, biological, chemical, and ecological processes occur. These processes all interact to determine the ecology found in and around coastlines (Leal et al., 2009). Urbanization and industrialization are affecting coastal areas at an alarming rate, deteriorating the quality of oceans, as well as rivers, and canals. This is primarily due to industrial, agricultural, and domestic sources releasing large amounts of chemical and biological waste into the surrounding water sources (Obura et al., 2019; Qin et al., 2008; Tu
et al., 2014; van Aswegen et al., 2019). The marine environment is not only influenced by
land-based activities, but also through shipping, oil- and gas mining, and fallout from atmospheric particles, further decreasing water quality in marine and coastal environments (Llewellyn et al., 2016; Meng et al., 2008).
Ships, being one of many polluting sources, can release massive amounts of sulphur and nitrogen oxide from their engines, where these pollutants are deposited back into the ocean's biogeochemical cycle. This is evident due to increased eutrophication and atmospheric pollution acting as indicators, that the Indian Ocean is being polluted. These two pollution sources can be linked directly to population increases around the edge of the Indian Ocean (Hood et al., 2015). The Food and Agriculture Organisation (FAO) as cited in Hood et al., 2015 further strengthens
this statement since they reported that the concentrations of nitrogen (N) and phosphorous (P) have increased dramatically since the 1970s.
The N and P enrichment phenomenon coupled with other anthropogenic activities (wastewater, urbanization, industrial effluent, and agriculture) can cause an imbalance within natural water systems, resulting in algal blooms (Anderson et al., 2002; Chen et al., 2013; Teichberg et al., 2010). This imbalance can cause the production of different species of phytoplankton and decrease the numbers of diatoms due to concomitant decreased silicate concentrations. When phytoplankton communities are phase-shifted, the food web can be altered, which could affect both human health and that of the aquatic organisms inhabiting the ecosystem (Dallas & Day, 2004).
Rivers and ground water are two additional sources responsible for carrying ever-increasing amounts of nutrients, carbon, and metallic elements into coastal areas (Pripp et al., 2014). Eutrophication caused by riverine runoff is generally low within the north and southwestern areas of the Indian Ocean, whereas high nutrient levels can be detected in the north-eastern parts. The Bay of Bengal is a good example of high nutrient loads entering the coastal environment from rivers and urbanized areas such as wastewater treatment, industries, leaching, and direct disposal within the environment (Mukhopadhyay et al., 2006; Paul et al., 2008). Another major influence on the Indian Ocean’s ecosystems is that of climate change. The complex interaction of biotic and abiotic systems within the Indian Ocean serves as an indication of how climate change can have both positive and negative implications concerning marine organisms (Hood et
al., 2015).
Aquatic organisms have long been used for monitoring pollution (He et al., 1998). Over the past few decades, the concentration of pollutants such as metallic elements within marine biota has been increasing (Kaladharan et al., 2005; Mubiana et al., 2005). These metals occur naturally within the environment at low concentrations, but due to anthropogenic activities, these concentrations have steadily been increasing above natural background levels (Hipfner et al., 2011) leading to potential health risks for aquatic organisms (García-Otero et al., 2013; Velusamy
et al., 2014). Metallic elements have been extensively researched through chemical, toxicological,
and ecological approaches (He et al., 1998). Recent studies have indicated that these compounds are entering the environment at a higher rate than in previous years (Lagerström et al., 2013; Srichandan et al., 2016; Yasin et al., 2010; Zhoa et al., 2012;).
Srichandan et al., (2016) stated that metal pollution is of concern due to the toxicity and persistence of these elements in the environment. Some elements have a tendency to assimilate or bioaccumulate in animals and eventually the food web (Achary et al., 2017; Yang et al., 2002). The magnitude of assimilation and/or bioaccumulation by animals in the marine environment is influenced by factors such as location, depth, distribution, trophic level, feeding habits, age, and size (Velusamy et al., 2014). These factors remain poorly researched and further research is needed to be better understand the effects caused by an increase in pollutants, together with natural oceanic drivers and anthropogenic stressors (Everaert et al., 2015).
the Arabian Peninsula, Somalia, Pakistan, and India (Figure 1.1) (Hood et al., 2015). Anthropogenic releases from industrial pollution and waste burning can also be found in these regions, especially at the Bay of Bengal and the Arabian Sea (Hood et al., 2015).
Figure 1.1: Map of Africa and India representing dust mass over the Arabian Peninsula, Somalia,
Pakistan, and India with a concentration scale. White arrows are wind direction. The scale indicates dust deposition (µg/m3 per day) (Windy.com).
When these atmospheric deposited metallic elements enter the environment through dust, they are redistributed through biogeochemical cycling and are frequently deposited into sediment. Sediment can thus be a target for the analysis of metallic elements. When these elements accumulate in sediment, they can later be reintroduced into the water column through upwelling events (Yang et al., 2002). Furthermore, metallic elements in low concentrations in water, combined with organic matter, are incorporated in phytoplankton, eventually forming part of the food web and can ultimately start to bioaccumulate (García-Otero et al., 2013).
Certain elements (copper (Cu), zinc (Zn), iron (Fe), chromium (Cr), and cobalt (Co)) are essential micronutrients needed for enzymatic reactions by producers, but they can also regulate primary productivity. By limiting primary productivity, the amount of CO2 that is regulated limits the nutrient
cycle within the given environment (García-Otero et al., 2013; Lagerström et al., 2013). Metal circulation in the ocean has complex interactions between biogeochemical processes in combination with physical characteristics. Biogeochemical data can therefore be used as an indication of what interactions are taking place in the water column (He et al., 1998). These interactions can furthermore be used as mechanisms of tracing pollutant pathways into and throughout the ocean (Lagerström et al., 2013).
Even though metallic elements can be used to trace pollution sources, a change in the ocean’s chemistry, circulation, and temperature causes a transfer of organisms to new regions possibly changing the food web dynamic there (Hood et al., 2015). These changes and unpredictability play a role in the structuring of many different biological communities that are found in coastal waters.
Two communities—phytoplankton and zooplankton—stand out when looking at the bottom of the food web. These two functional groups are responsible for several functions in the oceanic ecosystem (Leal et al., 2009). The density and biomass of zooplankton in surface waters normally correlates with phytoplankton. And, since the abundance of zooplankton is determined through phytoplankton, the abundance can be traced back to predator-prey interactions. Zooplankton feeds on phytoplankton; in turn, planktivorous fish and larvae feed on zooplankton (Leal et al., 2009). In this sense, zooplankton regulates the abundance of phytoplankton, and fish regulates the zooplankton biomass.
Other factors influencing the abundance of phytoplankton are light, temperature, nutrients, phosphates, nitrogen, and silica (Everaert et al., 2015). Strong tidal currents and upwellings cause mixing of the water column, disturbing stratification. This effect causes phytoplankton and zooplankton in coastal areas to be distributed throughout the water column. In deeper water, the introduction of excess nutrients, phosphates, and nitrogen can cause phytoplankton blooms as well as affect the ecology (Leal et al., 2009). The Indian Ocean may act as a model to indicate how climate change can influence the biogeochemistry and ecology of the world oceans through different factors, including that of zooplankton (Hood et al., 2015).
1.2. The Indian Ocean
According to Hood et al. (2015), the Indian Ocean is a unique ecosystem in many ways. Kojadinovic (2016) stated that very little research has been done in the Indian Ocean, especially about metallic elements. Furthermore, he concluded that organisms at the top of the food web are usually exposed to high concentrations of metallic elements through the food they eat, combined with bioaccumulation from water (Kojadinovic et al., 2007). Patterson et al. (2006) concluded similar stating that the eastern boundary of the Indian Ocean is less studied than the rest of the world’s oceans in terms of microzooplankton. In general, the Indian Ocean remains one of the world’s less-studied and under-sampled oceans when compared with the Atlantic and Pacific (Hood et al., 2015).
The John Murry Expedition was one of the first major expeditions to the Indian Ocean. This expedition took place in 1933-34 and mainly focused on the Arabian Sea where the first oxygen deficiency in mesopelagic activities was recorded (Hood et al., 2015). The overall general lack in research leads to many scientific questions arising and being unanswered, especially in terms of the zooplankton community and ecotoxicology of the Western Indian Ocean (WIO) (Hood et al., 2015). This lack in research is a recurring theme in literature.
1.2.1. Indian Ocean topography
ridges play an important role in depth, surface, and deep-sea circulation within the Indian Ocean (Hood et al., 2015).
In the Indian Ocean, seven ridge-basins dominate the ocean floor topography. These include the Arabian, Agulhas, Crozet, Madagascar, Mascarene, and Mozambique ridges in the WIO and central Indian Ocean. Along the eastern side of the Indian Ocean there are two main ridges found namely Wharton and the South Australia basin (Hood et al., 2015).
Three major rivers have broken through the ridges, discharging freshwater into the Indian Ocean. The Ganges River enters the Bay of Bengal, the Indus River enters the Arabian Sea, and the Zambezi River enters along the coast of Mozambique (Hood et al., 2015).
Surface circulation in combination with landmasses tends to increase the biological productivity (Sigman & Hain, 2012) in the Indian Ocean. This can be due to the interaction of nutrient areas around Islands, as well as nutrient runoff from Island regions, which can lead to nutrients and pollutants such as metallic elements to enter the ecosystem (Hood et al., 2015).
According to Hood et al. (2015), most of the suspended sediment that enters the Indian Ocean is from the Indian Subcontinent. This sediment load is of the highest when compared with the Indian, Pacific, and Atlantic Oceans. These sediment loads are generally deposited on continental shelves and associated slopes, and eventually into the abyss of the Indian Ocean. An example of this sediment deposit can be found along the coast of Somalia and Mozambique where the sediment deposition is more than a kilometre thick (Obura et al., 2019).
Due to the specific topography and geometry found within the Indian Ocean, in combination with wind-driven monsoons, the circulation becomes unique and complex in the tropical regions of the Indian Ocean (Hood et al., 2015). The seasonal complexity combined with centres where sediment enters the Indian Ocean plays an important role in the biogeochemical system of this ocean (Hood et al., 2015).
1.2.2. Indian Ocean currents
I discuss the currents of the region where I conducted my studies as an important background and context of the findings of my study. Throughout the Indian Ocean, there are a number of complex major currents (Figure 1.2). The South Equatorial Current (SEC) is the main current that carries water from the east towards the African continent. This current runs through the tropical region of the Indian Ocean where, on the eastern side of Madagascar, it branches into two currents forming the South East Madagascar Current (SEMC) and Northeast Madagascar Current (NEMC) (Groeneveld & Koranteng, 2017; Obura et al., 2019; Pripp et al., 2014).
Figure 1.2: Map of main oceanic currents of the West Indian Ocean together with current speeds
and eddies. Air temperature and cities are also included on the day the figure was created (15 November 2019) (Windy.com)
The SEMC and NEMC currents have an impact on the Mozambique Channel (MC) and Mozambique Current through shedding eddies into this channel. In the northern part of the MC, the NEMC breaks off south pushing eddies into the MC. The split tends to happen around the Comoros Islands. These eddies now travel through the MC along the coast of Mozambique and Madagascar (Figure 1.2) where it eventually breaks off back into the Indian Ocean, or join the greater Agulhas Current (AC) south along the east coast of South Africa (Barlow et al., 2013; Groeneveld & Koranteng, 2017; Hood et al., 2015; Obura et al., 2019; Potier et al., 2014). At the southernmost tip of Madagascar, the SEMC can either enter the MC or move back into the Indian Ocean as mentioned as eddies traveling along the western side of Madagascar (Hood et al.,
African Coastal Current (EACC) flows northwards forming part of the Somali Current (SC). [This information is relevant as it coincided with the time of sampling.] The SC then flows into the Arabian Sea where it influences the different monsoon seasons (Groeneveld & Koranteng, 2017; Hood et al., 2015). This SC also breaks off to feed back into the South Equatorial Counter Current (SECC) leading back into the Indian Ocean (Groeneveld & Koranteng, 2017). Between the Atlantic, Pacific, and Indian Oceans, the latter is the least understood in terms of circulation; this may be because the Indian Ocean has unique geomorphology, seasonal influences, and unique surface and deep-water currents, in combination with upwelling and downwelling events (Hood
et al., 2015; Lamont et al., 2014).
Water mixing also occurs within the MC. An example of this is the mixing of the Indonesian Throughflow (ITF) waters with waters of the SEC. This mixing of different water masses can be seen at different depths but is most prominent at the thermocline and other intermediate depths (Makarim et al., 2019). Hood et al., (2015) suggests that this mixing of water influences the physical and chemical properties of the Indian Ocean through the introduction of freshwater, and water from the Pacific Ocean. Furthermore, they suggest that the ITF can cause the exchange of physical and chemical properties as well as biological properties through the introduction of larvae, plankton, nutrients, and essentially the transfer of pollutants such as metallic elements.
Upwelling and downwelling zones greatly influence the biogeochemistry as well as planktonic ecosystems of coastal regions (Béhagle et al., 2014; Pripp et al., 2014). These influences can be traced back to boundary currents mixing coastal zones, impacting higher trophic levels and behaviour of organisms (Potier et al., 2014). Even though most of the currents in the Indian Ocean are permanent, some are mainly influenced by seasonal changes. Currents such as the SC, West Indian Coastal Current (WICC), and East Indian Coastal Current (EICC) starts flowing slower and eventually dissipates following which the flow reverses depending on specific seasons. The SC is especially known for its strength and direction reversal properties (Hood et al., 2015; Wang et
al., 2018).
The inclusion of warm water transport through the Indonesian Seas to the Indian Ocean plays a role in global thermoregulation. This water passes through the Indian Ocean and enters the Southern Atlantic Ocean through eddies breaking off from the greater AC at the tip of southern Africa (Lamont et al., 2014). The exchange of water through the Indian Ocean mostly takes place within the tropical regions of the SEC, but heat transport through the MC into the AC is important for thermoregulation of the global oceans (Hood et al., 2015).
The AC along the coast of South Africa is of importance due to the transfer of water from the Indian Ocean into the South Atlantic Ocean, carrying characteristics from the Indian Ocean into the South Atlantic Ocean through eddies and natural water transfer. Furthermore, strong associations can be found with upwelling events in the AC, MC, and Eastern Madagascar Current (EMC) (Lamont et al., 2014; Lutjeharms & Bornman, 2010).
1.2.3. The Mozambique Channel (MC)
In the WIO, the MC can be found between Mozambique and Madagascar flowing southwards from the northern tip of Madagascar towards South Africa (Jose et al., 2013; Potier et al., 2014). This current connects with the Agulhas Current and eventually breaks of into smaller eddies returning into the Indian Ocean but can also cross into the Atlantic Ocean through the break off
of eddies at the southern tip of Africa (Halo et al., 2014; Ternon et al., 2014a; Ternon et al., 2014b). In the northern part of the channel, the Comoros Islands can be found. Its geographical outline causes interesting flow patterns within the MC (Obura et al., 2019; Ternon et al., 2014a; Ternon et al., 2014b).
From a biogeographical point of view, the MC has drawn a lot of attention due to the existence of a complex current system (Mattio et al., 2016; Obura et al., 2019). These complex flow patterns can be ascribed to eddies in the MC. Another factor influencing the complexity of the eddies and circulation is that of the topography in the MC and Indian Ocean (Barlow et al., 2013; Obura et
al., 2019; Ternon et al., 2014b).
As mentioned earlier, the SEC divides into different currents, eventually forming the northwards flowing SC and the southwards flowing MC (Kai & Marsac, 2010; Obura et al., 2019). This leads to complex surface and bottom circulation, as also mentioned earlier. With this complex circulation and taking into consideration the shape of the Mozambique Channel, different processes occur due to the presence of upwelling and downwelling eddies (Béhagle et al., 2014; Ternon et al., 2014a; Ternon et al., 2014b). Even though the MC traverses the Mozambique coastal area, the SC and MC both possess different oceanographic properties (Groeneveld & Koranteng, 2017). This combination has an impact on upwelling regions as well as the biodiversity (Kai & Marsac, 2010).
Whereas coastal water mainly consists of two types of surface water such as Tropical Surface Water (TSW) and Subtropical Surface Water (STSW), tropical water within the Indian Ocean is known to have lower salinity and higher temperatures in surface water, whereas water in the STSW has higher salinity (Groeneveld & Koranteng, 2017).
1.2.4. Eddies
I discuss eddies in detail, as this may affect the metal compositions of zooplankton, the subject of my study. Groeneveld & Koranteng (2017) found that anticyclonic eddies are more prone to downwelling. Heat and oxygen is pushed down to deeper water layers, whereas cyclonic eddies are connected to upwelling resulting in higher chlorophyll concentrations as well as cooler nutrient-rich water being drawn up from the deeper water layers changing the characteristics of the water (Marsac et al., 2014; Pripp et al., 2014). In contrast, Hood et al., (2015) found that even though cyclonic eddies cause upwelling, they do sometimes have lower concentrations of chlorophyll and downwelling eddies sometimes have higher concentrations of chlorophyll. This leads to nutrients being transported between the African coasts and Madagascar in the MC (Groeneveld & Koranteng, 2017; Halo et al., 2014; Obura et al., 2019; Ternon et al., 2014a).
It is well known that eddies play a role in the biological structuring of certain areas (Ternon et al., 2014a). This can be seen by studying the lowest levels of the food web including that of chlorophyll, plankton, and zooplankton distributions in the Indian Ocean (Béhagle et al., 2014; Halo et al., 2014; Marsac et al., 2014; Obura et al., 2019).
production, and accompanying secondary production, which is supported by the higher abundance of copepod and euphausiid nauplii found in the cyclonic eddies when compared with the anticyclonic eddies. (Groeneveld & Koranteng, 2017; Halo et al., 2014; Marsac et al., 2014; Obura et al., 2019)
Furthermore, primary production in the MC mostly increases due to increases of nutrients (and presumably metals as well) retrieved from coastal areas instead of eddies being the main source of nutrient input of deep-water nutrients to the euphotic zone (Barlow et al., 2013; Hood et al., 2015; Lamont et al., 2014; Marsac et al., 2014). The MC eddies play an important part within the ecosystem through shaping the behaviour of organisms as well as impacting the biodiversity and foraging of higher trophic levels (Hood et al., 2015; Marsac et al., 2014; Obura et al., 2019). Eddies therefore, are likely to have an effect on metal concentrations in zooplankton.
The quantity and strength of eddies found within the MC can be strongly affected by the SEC which could, in turn, have a greater impact on higher trophic levels feeding in this area. This, in turn, would affect the transport of nutrients (and probably metals as well) between regions within the MC (Hood et al., 2015; Lamont et al., 2014; Obura et al., 2019). Halo et al., (2014), agreed with this statement as they found that anti-cyclonic eddies were predominantly found along the coast of Mozambique whereas cyclonic eddies predominantly travelled along the Madagascar coastline in an easterly direction within the Mozambique channel transporting nutrients and possible pollutants along the way.
1.2.5. Upwellings
In terms of energy, upwelling is a mode of energy transfer between the deep parts of the ocean, surface water, and the atmosphere. This energy transfer causes nutrients to be brought up from the sediment or deep ocean to be transferred into the food web (Sigman & Hain, 2012).
Malauene et al. (2014) stated that between the months of August and March every year, increased chlorophyll concentrations are found along the coastal region of Angoche (Figure 1.2) in Mozambique (Marsac et al., 2014). This is primarily due to increased wind-driven upwellings during these periods. These wind-driven upwellings can also be seen at the southern tip of Tanzania near Mtwara. Specifically, the combination of wind, eddies colliding with coastal shelves, and the seafloor causing an upwelling region along Angoche; whereas wind-driven upwellings are also seen along the Comoros basin (Groeneveld & Koranteng et al., 2017; Obura
et al., 2019).
Along the Mozambique coast, an inshore coastal current can be found flowing in a northerly direction. This specific current is known as the Delagoa Bight (DB) that mainly consists of eddies interacting with the area's topography to cause upwelling events on the Mozambican shelf (Groeneveld & Koranteng et al., 2017; Lamont et al., 2014; Potier et al., 2014). Another input of excess nutrients can be traced back to the Zambesi River causing the Sofala Bank to be an area high in nutrients, resulting in the area being impacted by not only the river outflow but also that of passing eddies along the shelf. Since there is an increase in nutrients (and presumably metals as well), primary productivity increases, thus leading to enhanced productivity throughout the trophic levels (Groeneveld & Koranteng et al., 2017; Pripp et al., 2014). Groeneveld & Koranteng (2017) further highlights the biological importance of this area, noting that the Sofala Bank is an important distribution area for pelagic fish species.
It is well understood that the main source of increased primary production is that of nutrient availability and light intensity (Sigman & Hain, 2012). Mechanisms such as rivers tend to supply high concentrations of nutrients into the ocean that in return enhances primary production (Pripp
et al., 2014). In the WIO, there are mechanisms that affect the biomass, distribution, and
abundance of organisms (Potier et al., 2014). These mechanisms are, to name a few, oceanic upwellings, wind-driven upwellings, eddy circulation, and river inflow, which in turn causes mixing of water layers and therefore enhanced stratification (Groeneveld & Koranteng et al., 2017; Obura
et al., 2019). Not only do eddies cause vertical stratification along the coast, but stratification can
also be found within the open ocean where nutrients (and presumably metals) are transferred to different layers due to cyclonic eddies causing upwellings (Jose et al., 2013; Lamont et al., 2014; Lebourges-Dhaussy et al., 2014).
Permanent upwelling zones can be found along the equator in the Atlantic and Pacific oceans. In contrast, the Indian Ocean has upwelling zones situated at higher and lower latitudes. This means that upwelling regions can be found for example along Somalia, Seychelles, and the northern tip of Mozambique (Hood et al., 2015). Of the coast of Oman and Somalia, an extreme upwelling region can be found which is mainly produced by the Asian-African monsoon (Hood et al., 2015).
The WIO is unique worldwide due to rich geophysical mechanisms that cause upwellings and this in turn results in the WIO differing vastly from the eastern side of the Indian Ocean (Hood et al., 2015). This complexity may have an influence on metal concentrations and compositions in zooplankton of the WIO.
1.2.6. Ocean zonation
The northern part of the Indian Ocean has many freshwater influences especially in the Bay of Bengal, which may lead to increased stratification (Hood et al., 2015). The northern Indian Ocean is also known for its oxygen-depleted water that influence benthic organisms as well as primary productivity (Marsac et al., 2014). Dead zones are of major concern within coastal areas and the open ocean. These dead zones are formed by an increase in primary production leading to increased consumption of dissolved oxygen by primary producers and microbial communities (Hood et al., 2015). The occurrences of dead zones in the Indian Ocean are on the rise, especially in the north (Hood et al., 2015).
Deoxygenation has received increased attention during the last decade due to increased eutrophication. This, in combination with lower ventilation, increased stratification, and reduced upwelling places more stress on aquatic biota (Hood et al., 2015). Furthermore, deoxygenation may lead to an expansion of intermediate water layers with conditions favouring increased loss of bioavailable nitrogen under anoxic conditions via denitrification and anaerobic ammonium oxidation reactions (Sigman & Hain, 2012). Moreover, deoxygenation will enhance production of climate-relevant trace gases such as N2O, CH4 and dimethylsulfide that are released to the
atmosphere from upwelling regions in the northern Indian Ocean. Mesopelagic fish populations may therefore be threatened by a reduction in suitable habitat as respiratory stress increases (Hood et al., 2015).
affect primary and secondary productivity (Sigman & Hain, 2012). Coastal areas are more susceptible to environmental changes due to total depth not being deep enough to maintain stability (Hood et al., 2015).
Finally, the marine water column can be stratified in different layers according to nutrients, sunlight, temperature, and oxygen. Each layer houses different organisms that possess the ability to move between layers. In trophic networks, certain organisms remain important to ensure a healthy environment. Primary producers, secondary producers/consumers, and top predators are all-important within the epipelagic and mesopelagic layers (Béhagle et al., 2014; Hood et al., 2015; Lamont et al., 2014; Sigman & Hain, 2012).
1.3. Biogeochemical cycles
There are three main biogeochemical cycles.
1.3.1. The carbon cycle
Carbon monoxide and carbon dioxide (CO2) are the two most common forms of inorganic carbon
found within the environment. Carbon dioxide fixation is the starting point of the carbon cycle and involves the alteration of CO2 by changing it into organic matter. Plankton, bacteria, and protists
play a fundamental part in the marine environment in terms of the ocean’s carbon cycle. Phytoplankton are mainly found in surface water, and bacteria found beneath the euphotic layer, due to bacteria’s ability to fix carbon under anoxic conditions in the absence of light (Sigman & Hain, 2012). These organisms are responsible for approximately half of the carbon fixing that takes place on earth. Apart from carbon fixing, phytoplankton is also a primary producer of dissolved organic matter (DOM) in marine ecosystems (García-Otero et al., 2013; Willey et al., 2011). With different stratification activities taking place in the world’s oceans, there are certain areas with low stratification that can result in massive algal blooms under the right conditions (Patterson, 2006).
This constant rise in CO2 in the atmosphere causes not only ocean acidification but also global
ocean warming. With increased water temperature comes a decrease in stratification, causing a decrease in upwelling; this in turn leads to nutrients (and certain trace elements) from deep water and sediment not being able to reach the surface layers of the ocean. With a decrease in nutrient availability, decreased primary productivity and biogeochemistry may occur. This enormous change in the ocean's natural cycles can affect denitrification and eventually food webs and fisheries (Hood et al., 2015).
1.3.2. The nitrogen cycle
One of three major oxygen-depleted zones can be found in the northern part of the Indian Ocean with oxygen almost reaching a concentration of zero in waters of the Arabian Sea. This may disrupt the biogeochemical processes in the Arabian Sea and Indian Ocean. Approximately 20% of the world’s denitrification takes place in the Arabian Sea. The Arabian Sea has been identified as an area of global importance in terms of open-ocean denitrification, but the Bay of Bengal is also of concern due to decreasing oxygen concentrations. Although low oxygen concentrations are found, the Bay of Bengal’s threshold is still just above the threshold where denitrification starts to occur (Hood et al., 2015).
Algae, mainly cyanobacteria, convert atmospheric nitrogen into ammonia that can serve as another food source for phytoplankton (Sigman & Hain, 2012). Approximately 30-40% of nitrates
that are found within the Arabian Sea are produced from the fixation of atmospheric nitrogen, especially in euphotic zones. Nitrogen fixation is estimated to support up to 50% of new production in areas where low primary productivity is found (Hood et al., 2015). Organic nitrogen fixation is mainly produced by two main groups of organisms; bacteria and archaea. These organisms are the main nitrogen fixers within the environment with lightning strikes, volcanic activity, and fertilizer manufacturing also contributing (Willey et al., 2011). Even though being such an important event, there is still not enough data on nitrogen fixation to quantify with certainty what the total input of nitrogen is to the Indian Ocean (Sigman & Hain, 2012).
An increase in nutrients in the water will not only have dramatic effects on the biogeochemical cycle of the ocean but will also impact coastal food webs. As earlier stated, increased human population and coastal development have had and continuous to have severe negative effects on coastal environments. With increased nutrient effluent entering the marine environment, the chances of food webs and natural processes becoming perturbed greatly increase (Sigman & Hain, 2012). This leads to a further decrease in pH in the water column. Additionally, ammonia is transformed into ammonium that can influence biological interactions such as the microbial loop and phytoplankton interactions (Hood et al., 2015).
1.3.3. The microbial loop
Over the decades, marine microbes have been able to adapt to continually changing physical and chemical parameters driven by anthropogenic activities. Changes in water temperature and chemistry will inevitably affect the Indian Oceans’ microbial communities. There are few bacterial species in high abundance in these ecosystems. Changing any physical or chemical parameter can drastically influence the distribution and composition of the abundant bacteria, and in turn affect the important roles they play in various biological processes (Hood et al., 2015). Bacteria involved with nitrogen fixation and denitrification can start to bloom, become toxic, and spread, eventually affecting the nitrogen cycle and the total chemistry of the water column (Hood et al., 2015).
The microbial loop starts in the photonic layer, but mainly occurs underneath this layer, due to the bacteria’s ability to function in low light. Processes such as remineralization take place through microbes, protists, flagellates, and microzooplankton that help to reintroduce nutrients into the photonic layer that in turn helps with the growth of phytoplankton. Since biological, chemical, and microbial activities are all linked, this redistribution process best describes the proper functioning within the environment (Patterson, 2006).
1.4. Trace metals in the Marine Environment
Just as the carbon, nitrogen, and microbial interactions interacts with each other, so does this affect how trace metals behave in water. With a worldwide increase in pollution, metallic elements have increased leading to growing concerns for human health. Metallic elements occur naturally or are present due to anthropogenic inputs to all ecosystems (Echeveste et al., 2016; Qin et al., 2008). It is therefore inevitable that these metallic elements ends up in the marine environment, where some of the elements are highly toxic and can start to bioaccumulate in marine organisms (Achary et al., 2017).
needed by various organisms. From a biological context, metallic elements can be classified as essential or non-essential (García-Otero et al., 2013; Twining et al., 2011). There are a number of ways for essential elements such as Fe to enter the marine environment; these include atmospheric dust, resuspension, and hydrothermal vents to name but a few (Nishioka et al., 2013). Elements such as lead (Pb), and mercury (Hg) do not have a specific biological function (therefore non-essential), and as such can be toxic with increasing concentrations. With a change in climate and increased anthropogenic inputs, the concentration, distribution, and availability of metallic elements in the ocean are continuously changing, including interactions with carbon, nitrogen, and bacteria. The distribution and concentration of metallic elements are controlled by certain factors such as biological uptake, binding to organic or inorganic particles, and deposition into marine sediment (Aparicio-González et al., 2012).
An example of this can be found along the coast of Vietnam were high metal concentrations have been found along the coast as well as in a variety of environmental samples. This raises concern due to the large human dependence on biota from contaminated environments (Tu et al., 2014).
Water's composition is influenced by its specific physical-chemical properties. In terms of metals in water, the composition is also influenced by the availability of metals as well as the ability to be able to bind to biotic ligands. This means that certain metals can be toxic to organisms such as fish since they interfere with the physiological Ca and Na/K pump. This can in time lead to the swelling of fish gills and eventually death (Fisher & Hook, 2002). With an apparent shift in the global distribution of organisms, —especially poleward—might have effects on higher trophic levels, since food sources are shifting, eventually redistributing metallic elements from one region to another (Hood et al., 2015).
The effect of pollutants occurring naturally has gained more attention in recent times, and remote areas such as the Arctic and Antarctic have become places of concern due to increased anthropogenic introduction of metals into food webs (Kojadinovic et al., 2007; Nishioka et al., 2013). This increased interest shows that the modern situation of pollution is a problem and up to date research is urgently needed (Echeveste et al., 2016).
1.4.1. Metabolic and physiological influences of metals
Out of most of the pollutants that can be found in coastal and estuarine sediment, metallic elements are known to be the most persistently present (Meng et al., 2008; Qin et al., 2008; van Aswegen et al., 2019). For this specific reason, they can be used as indicators of what is happening in the environment.
Physical, chemical, and biological dispersal plays an important part in what happens with these metallic elements once they enter the marine environment. Organic matter that enters the environment can be either consumed, sink to the seabed, or be demineralized. These factors help with the regulation of trace metals in the biogeochemical cycles (Srichandan et al., 2016).
Metallic elements such as Mn, Fe, Co, Ni, Cu, and Zn play important roles in the marine environment, especially in biogeochemical processes. Ambient essential elements can be influenced by nutrients used for plankton growth since these elements can become exhausted in surface water and enriched at depths due to assimilation and accumulation, sinking, and subsequent remineralisation at deeper depths. Furthermore, there seem to be noticeable trends in the composition of metallic elements that are found within certain taxonomic groups, due to the
vertical distribution of metallic elements through biological and ecological processes in plankton. Even though this plays a major role in animals, the availability of these elements can be influenced, but availability and specific uptake mechanisms of organic compounds are not fully understood (Twining et al., 2011).
The Arctic marine ecosystem is a good example of an ecosystem being impacted by metal pollution. This ecosystem has been receiving more attention ever since metallic elements have been found to be contaminating the ecosystem. Ritterhoff and Zauke (1997) stated that arsenic (As), Cd, Pb, Zn, vanadium (V) and antimony (Sb) in the Arctic accounts for approximately 6% of Eurasia’s emissions. In the Arctic food web, zooplankton plays a crucial role since they are a food source for marine mammals, birds, and fish. Additionally, zooplankton can also contribute to bioaccumulation of these elements in higher trophic levels. Due to these dynamics, zooplankton is a good biomonitor to assess the presence and abundance of these elements in lower trophic levels in aquatic environments (Ritterhoff & Zauke, 1997).
Fisher and Hook (2002) found that gold (Au) and cadmium (Cd) can decrease the reproduction of zooplankton; but when these metallic elements were taken up from an aqueous solution, no reproductive effects were observed. Cadmium, Au, and Hg that have accumulated in organisms from aqueous solutions tend to accumulate on the exoskeleton of zooplankton, but metals ingested accumulated within the organism itself, thereby causing effects (Fisher & Hook, 2002).
Mercury is a well-known non-essential element and especially toxic at above background thresholds (ATSDR, 1999). Mercury can either occur naturally or enter the environment through anthropogenic inputs. Mercury’s toxicity is determined by its chemical form and the concentrations in the environment. It occurs either in elemental, organic, or inorganic form. The most toxic of the three being organic mercury (methylmercury); for this reason, it is important to determine the specific type of Hg. Since Hg can be transported by air, the circulation time and the chemical transformation to methylmercury can cause organisms in remote areas of the world to be exposed to Hg, along with other pollutants (Pacheco et al., 2010).
1.4.2. Oceanic nutrient transport
Mesoscale eddies change the biogeochemical process through physical, chemical, and biological interactions (Béhagle et al., 2014). Eddies (cyclonic or anticyclonic) can influence the nutrient supply needed by organisms. Cyclonic eddies redistribute nutrient-rich water (deep water) into the eutrophic zone (Malauene et al., 2014). In contrast, anticyclonic eddies displace water, nutrients, and chlorophyll to collect on the outskirts of the eddy ( Béhagle et al., 2014; Kolasinski
et al., 2012). Tropical parts of the ocean are usually limited in terms of nutrients. Organisms living
in these areas are dependent on nutrient cycling and the vertical migration or redistribution of nutrients from nutrient-rich water (Kolasinski et al., 2012). Nutrients from nutrient-rich sectors or layers can also be transported to areas or layers that are nutrient-poor, enhancing primary production and promoting biodiversity increases (Jose et al., 2013; Malauene et al., 2014).
An example of nutrient-limited waters is that of the MC. Although these waters aren’t nutrient-rich and have low primary productivity, they support large numbers of top predators (Kolasinski et al.,
Huggett (2014) stated that during daytime, large gatherings of zooplankton occur at the surface of the MC, in combination with numerous Greater Frigate Birds (Fregata minor) which feed in this area especially with the association of zooplankton on the edges of eddies. Upwelling in the centre of cyclonic eddies, especially in oligotrophic systems, supply high nutrient levels leading to increased primary production, and increased zooplankton abundance and biomass (Huggett, 2014; Lebourges-Dhaussy et al., 2014;Malauene et al., 2014).
In the MC, general information of zooplankton is lacking. Knowledge on general biomass, community structures, and the distribution of zooplankton for eddies and between eddies are needed. Knowledge like this is needed to understand the fundamentals of normal functioning of mesoscale ecosystems. This knowledge, linked with feeding behaviour between trophic levels, will help with the understanding of how trophic transfer (of metals) occur (Huggett, 2014).
1.4.3. River runoff
Freshwater differs from ocean waters in many respects, mainly lower salinity. According to Groeneveld & Koranteng (2017), the WIO has been categorized in three parts namely North of 18 degrees south, central with increased riverine runoff, and south of 24 degrees with moderate influence of freshwater. The Zambezi River enters the ocean at approximately the central part along the coast of Mozambique. The Zambezi River has an extended influence on the salinity and nutrients in the ocean surface layer up to approximately 30 m and 50 m deep in stormy or rainy seasons stretching up to 50 km offshore (Nehama & Reason, 2014; Pitcher et al., 2008).
River plumes in the oceans change the characteristics of the area they flow into due to the enhanced terrestrial nutrients causing possible eutrophication, an inflow of sediment, and river-borne pollutants (Pripp et al., 2014). Seasonal influences of riverine flow change production in the Indian Ocean (Hood et al., 2015). Increase in nutrients leads to increased primary productivity and eventually enhances local fish populations (Hung et al., 2014). However, pollutants are also taken up by biota.
1.5. Role of plankton
Plankton is a general term that commonly refers to marine organisms that cannot escape currents but instead rely on currents for transport. Plankton includes phytoplankton, zooplankton, bacteria, and viruses (Willey et al., 2011). Taking all of this into consideration, approximately 98% of the oceans living biomass is made up of plankton that produce about half of the world’s oxygen. The other 2% is mainly comprised of organisms that are not reliant on currents for movement known as nekton; these include squid, crab, fish, and mammals (Groeneveld & Koranteng, 2017).
Phytoplankton are primary producers using sunlight and nutrients. Since they depend on sunlight, they are mostly found in the euphotic layer. Even though phytoplankton needs light and nutrients to thrive, they also depend on carbon dioxide, water depth, temperature, and grazers, resulting in differences in seasonal distribution (Groeneveld & Koranteng, 2017). Therefore, the increase in complexity of pollutants due to anthropogenic inputs can eventually have an effect on oceanic organisms leading to an impact on the global carbon and nitrogen cycles, bacterial activity and compositions, and ocean productivity (Echeveste et al., 2016). On the other hand, exposure of phytoplankton to contaminants such as metallic elements increases their tolerance towards these pollutants (Echeveste et al., 2016), leading to more complex dynamics.
Secondary producers/consumers in the marine environment mainly consist of zooplankton that feed on phytoplankton and small zooplankton (Marsac et al., 2014). Zooplankton are mainly crustacean and gelatinous organisms that depend on currents to move long distances. These include some larval stages of fish and molluscs that later tend to move out of the currents and either become free-living or migrate to the benthic environment (Groeneveld & Koranteng, 2017).
Although being restricted to currents for migration and distribution, a mass vertical movement takes place on a diel basis. In the epipelagic and photic zones, zooplankton can strongly influence the vertical transfer of elements (Battuello et al., 2016; Groeneveld & Koranteng, 2017; Marsac
et al., 2014; Potier et al., 2014).This vertical migration towards surface waters takes place at night
when predation risk is lower. One of the reasons for this daily migration is to feed on nutrients and food rich surface waters (Groeneveld & Koranteng, 2017).
Zooplankton can be categorised according to size; five size categories are generally recognised. These are nano-, micro-, meso-, macro-, and megaloplankton. Nanoplankton ranges between 2-20 µm, microplankton between 2-20-2-200 µm, mesozooplankton between 0.2-2-20 mm, macrozooplankton between 2-20 cm, and megaloplankton between 20-200 cm. Mesozooplankton consists mostly of crustacean zooplankton commonly sampled with bongo nets with 200-300 µm mesh (Groeneveld & Koranteng, 2017).
Four main ecological functions are ascribed to microzooplankton namely: grazing to regulate bacteria populations, nutrient regulation, transfer of organic matter and energy to higher trophic levels, and finally, assisting with primary productivity (Paterson, 2006). They may also cause to lure fish to areas where zooplankton are found in large numbers (Battuello et al., 2016). Although these animals are crucial for the marine environment, the information about the interaction these animals have with pollutants is very scarce (Ziyaadini et al., 2016).
Oligotrophic waters tend to have a lower zooplankton biomass than that of eutrophic waters (Marsac et al., 2014; Patterson et al., 2006; Pripp et al., 2014). According to Ziyaadini et al. (2016), there are three main interactions with pollutants:
• Pollutants can have a toxic effect on zooplankton being either lethal or sub-lethal, • Zooplankton can change the characteristics of the pollutants,
• Zooplankton can influence how pollutants are biomagnified throughout the trophic levels. Due to these interactions, it is important to understand the way pollutants and zooplankton interact to determine fate and effects of both (Battuello et al., 2016). Therefore, understanding zooplankton toxicology can lead to a better understanding of what impact pollutants may have on higher trophic levels and what processes in the biogeochemical cycles are influenced (Achary et
al., 2017; Battuello et al., 2016; Marsac et al., 2014).
1.5.1. History of zooplankton research in the Indian Ocean
The first recorded collection and study of zooplankton in the Indian Ocean was in 1857 to 1859. This collection was part of a circum-global scientific expedition, while other collections took place
place along the coast of southern Mozambique and along the eastern coast of South Africa. Zooplankton sampling only recurred during surveys taking place from 2007 onwards using bongo nets in combination with vertical multi-nets (Groeneveld & Koranteng, 2017).
Seven multidisciplinary expeditions were undertaken between 2007 and 2010 to better understand better the mesoscale eddies of the MC. These were important studies, because they helped with our understanding of the Indian Ocean’s productivity, especially in the WIO (Groeneveld & Koranteng, 2017; Lamont et al., 2014). Ternon et al., (2014a) also remarked that information about the zooplankton from the Mozambique Channel is rare.
Even though these studies were conducted, the most important and thorough expedition for zooplankton collection was during the first International Indian Ocean Expedition (IIOE) in 1957. Zooplankton samples were collected for the IIOE in the upper 200 m using a standard oblique bongo net with a mesh size of 330 µm.
1.5.2. Trace metals in Zooplankton
One of the many reasons metallic elements have received attention is because they play a role in physiological functions (Section 1.4.1) (Pempkowiak et al., 2006). High amounts of metals can enter the marine environment but the eventual concentrations can be relatively low due to dilution (Pempkowiak et al., 2006). Both water and food contribute to the assimilation and/or accumulation of these elements by organisms. Trophic transfer plays an important role in metallic element accumulation (Zauke & Schmalenbach, 2006). Even though an increase in the concentration of certain metallic elements can be toxic such as in the case of nonessential metals, essential metal concentrations can have a positive effect at low concentrations. If any metal, nonessential or essential, exceeds certain concentrations it will become toxic (Battuello et al., 2016).
In recent years, an increase in metallic element information can be seen, especially in regions such as the North Sea, Greenland Sea, and Weddell Sea (Zauke & Schmalenbach, 2006), as well as the North Atlantic and Pacific oceans, but little research has been conducted within the WIO (Lebourges-Dhaussy et al., 2014). Worldwide, sampling of zooplankton have been used to determine where “hot spots” for zooplankton are, as well as to determine the amount of metallic element contamination in coastal areas (Pempkowiak et al., 2006). These organisms especially close to coastal regions are exposed to elevated amounts of contaminants from inland sources (Battuello et al., 2016). Essential and nonessential metals have been tested by Battuello et al. (2016), but no concentrations were found in zooplankton that were high enough to be of concern.
Metallic elements are redistributed into deeper water through zooplankton defecation. These elements can remineralise and dissolve. By assessing the environmental quality in terms of metallic elements in seawater, the availability of these elements is of importance since a high concentration can have toxic effects (Battuello et al., 2016).
Within marine organisms, the accumulation patterns and accumulated concentration can vary between organisms of the same species. For example, different species of zooplankton from the same area have been found with different metallic elements concentrations (Zauke & Schmalenbach, 2006). Zooplankton can be used as biomonitors since they have a wide distribution, occupy different trophic positions, have high abundance, and have a high affinity for assimilating and/or bio-accumulating metals (Battuello et al., 2016).
The role of zooplankton in the biogeochemical process is well known, particularly the redistribution of metallic elements through the water column. Due to this redistribution and high biomass and spatial distribution, numerous studies have used zooplankton as biomonitors (Zauke & Schmalenbach, 2006). Zauke & Schmalenbach (2006) found high concentrations of Cd in zooplankton from the Arctic region. Pempkowiak et al. (2006) found samples of zooplankton contained detectable concentrations of Al, Mn, and Hg. However, there may have been some contribution from inorganic matter analysed together with the zooplankton. Pempkowiak et al. (2006) found that even though the concentration of metals within the Baltic Sea was small, the sediment layers were enriched with cadmium, lead, zinc, copper, and mercury.
In the ocean's water column, zonal patterns can be seen. This physical zonation can be contributed to fluctuating salinity and temperature across continental shelves. Even though zonation occurs, it is not a definitive barrier separating communities of zooplankton but rather increases the diversity of zooplankton communities (Schultes et al., 2013).
Since plankton can be used as good bioindicators of environmental change, more research and monitoring programs are recommended to determine the effects of pollutants on these ecosystems (Groeneveld & Koranteng, 2017). There have been many studies conducted on the distribution of metals and zooplankton along Indian coastal waters (Srichandan et al., 2016) but none in the WIO. Therefore, studies that focus on metallic elements within this region, especially within zooplankton, are important.
1.6 Aim and objectives
• Characterise the metal content and relative compositions of zooplankton of the WIO • Map and interpret the distribution of metals
• Identify zooplankton as “hot spot” indicator Objectives
• Collect samples from various sites and depths along transects in the WIO • Measure concentrations of metals and metalloids
• Assess metals in zooplankton as a spatial bioindicator
Chapter 2: Materials and methods
2.1. Ethical approval
Collection and analyses of samples was approved by the ethics committee of the North-West University (NWU) (NWU-01936-19-A9).
2.2. Study areas
Three study regions in the WIO were identified for sampling of zooplankton for metal analyses. Areas were classified according to the influence of three different oceanic currents. Samples were taken in the Mozambique Channel (MC) off the coast of Mozambique, in the East African Counter Current (EACC) of the coast of Tanzania, and in the South Equatorial Current (SEC) around the islands of Comoros, forming part of the WIO (Figures. 2.1, 2.2, 2.3, 2.4). The sampling was made possible due to participating in two Second International Indian Ocean II Expedition (IIOE 2) cruises. These cruises took place during October 2017 and June 2018 (Table 2.1; 2.2, 2.3). Very little research has been conducted on zooplankton in the WIO and even less has been conducted off the coasts of these regions.
The seas of the coasts of Mozambique and Tanzania are known for shipping, fishing, cities, agriculture, coastal mining, natural gas extraction, and oil drilling (Bosire et al., 2016; Llewellyn et
al., 2016). According to the UNDESA (2019) database, approximately 110 million people live in
the countries along the MC. Of the four bordering countries, Tanzania has 58 million people, followed by Mozambique with 30 million, Madagascar with a population of 27 million, and Comoros with approximately 850 000 people (Obura et al., 2019).
Obura et al., (2019) stated that the coastal development has been increasing at approximately double the predicted rate. This is mainly influenced by urbanization since these coastal areas have abundant natural resources. This is evident when looking at how many people are supported by fisheries alone. Approximately 56 000 people work in fisheries in Tanzania, with almost five times that number (280 000) in Mozambique (Obura et al., 2018).
Figure 2.1: Locations of all hydrographic stations sampled during 2017 and 2018 within the MC,
EACC, and SEC. Sampling began at Beira and ended just above Tanga. There were 29 transects running perpendicular to the coast and 94 stations were sampled for zooplankton.
Mozambique Tanzania Comoros Dar es Salaam Mtwarra E AC C SEC Rufiji River Ruvu River Grand Comoros Anjouan Moheli
2.2.1. Mozambique Channel: MC (Mozambique)
Mozambique has great and diverse mineral resource potential and is viewed an important exporter of raw materials, in particular coal, aluminium (Al) and gold (Au) (Marin et al., 2016). According to the World Wildlife Foundation (WWF) (2018), 58 900 km2 of Mozambique is under
contract for oil and gas, with many of these located along the Mozambican coastline (Obura et
al., 2019). The study area falls in the greater area known as the Sofala Bank stretching from Beira
21°S in the southern parts of Mozambique up to Angoche 16°S in the northern part of Mozambique (Malauene et al., 2018).
Figure 2.2: Locations of all hydrographic stations sampled during October-November 2017 in the
Mozambique Channel. Sampling began at Beira and ended just north of Angoche. There were 14 transects running perpendicular to the coast and 39 stations. Zooplankton was sampled at every station along each transect.
Table 2.1: Station coordinates for every sample in the Mozambique Channel for 2017.
Grid Latitude (degrees-south) Longitude (degrees-east) Year
M1-02 -20.31533333 35.3075 2017 M1-04 -20.56283333 35.54583333 2017 M1-06 -20.81533333 35.77816667 2017 M1-08 -20.93283333 35.90433333 2017 M2-01 -19.806 35.52316667 2017 M2-03 -19.993 35.6975 2017 M2-07 -20.42516667 36.11433333 2017 M2-10 -20.67983333 36.35466667 2017 M3-01 -19.31566667 35.75383333 2017 M3-03 -19.62766667 36.04916667 2017 M3-05 -19.87583333 36.28666667 2017 M3-07 -20.06333333 36.46866667 2017 M4-01 -19.091 36.23866667 2017 M4-02 -19.21566667 36.35416667 2017 M4-06 -19.6475 36.77183333 2017 M4-08 -19.83466667 36.94683333 2017 M5-04 -19.11633333 36.95966667 2017 M5-06 -19.23766667 37.08016667 2017 M6-01 -18.40483333 36.978 2017 M6-04 -18.716 37.27333333 2017 M6-09 -19.02383333 37.5665 2017 M7-01 -18.017 37.30116667 2017 M7-04 -18.26816667 37.53766667 2017 M8-05 -17.96916667 37.96916667 2017 M8-07 -18.15616667 38.15616667 2017 M9-05 -17.81716667 38.492 2017 M10-01 -17.25766667 38.64766667 2017 M10-03 -17.40383333 38.7935 2017 M11-01 -17.102 39.19033333 2017 M11-03 -17.236 39.31416667 2017 M11-04 -17.38916667 39.431 2017 M12-01 -16.66316667 39.75416667 2017 M13-02 -16.38366667 40.17316667 2017 M13-04 -16.57433333 40.3425 2017 M14-01 -15.91883333 40.42 2017 M14-03 -16.03733333 40.53 2017 M14-04 -16.1635 40.64633333 2017
2.2.2. East African Coastal Current: EACC (Tanzania)
Tanzania consists mainly of a large mainland sector and three major islands namely; Zanzibar, Mafia, and Pemba. Tanzania has a coastline that stretches from the northern border against Kenya towards the southern border of Mozambique. This stretch of coastline is approximately 800 km long and consists of a narrow section along the coast towards Kenya. The coastal section on the mainland consists mainly of thick sedimentary rock layers (Masalu, 2002).
In terms of mining and exporting of raw materials, Tanzania has become one of the most invested countries as well as one of Africa’s top gold producing countries, next to South Africa (Bryceson
et al., 2012). Tanzania made a gross income of approximately US $1.4 billion in 2009 on gold
exports alone, with Tanga, being one of the main mining regions. Mtwara is known for its variety of gemstone mines. Both mining regions are close to the (Bryceson et al., 2012). Near Dar es Salaam, an increase in sand mining has been observed, especially in local streams (Masalu, 2002).
Figure 2.3: Locations of all hydrographic stations sampled during October-November 2017, and
Tanga. There were 15 transects running perpendicular to the coast and 34 stations. Zooplankton was sampled at every station along each transect.
Table 2.2: Station coordinates for the East African Coastal Current for 2017-2018.
Grid Latitude (degrees-south) Longitude (degrees-north) Year
T1-01 -10.43 40.50666667 2017 T1-03 -10.42 40.67533333 2017 T1-05 -10.42 40.84266667 2017 T2-01 -9.97 39.84133333 2017 T2-03 -9.96 40.09483333 2017 T6-02 -8.03 39.92716667 2017 T8-01 -7.08 39.62383333 2017 T8-05 -7.06 39.95916667 2017 T8-07 -7.05 40.12833333 2017 T9-02 -6.6 39.41416667 2017 T9-04 -6.59 39.58316667 2017 T-A2 -5.27 39.24066667 2018 T-A3 -5.44 39.187 2018 T-A4 -5.71 39.1095 2018 T-A5 -5.93 39.07033333 2018 T-A6 -6.14 38.99233333 2018 T-A7 -6.26 39.00583333 2018 T-A8 -6.49 39.24266667 2018 T-A9 -6.67 39.35466667 2018 T-B1 -7.08 39.58633333 2018 T-B2 -7.09 39.6795 2018 T-B3 -7.08 39.7305 2018 T-B4 -7.08 39.80916667 2018 T-C1 -8.17 39.74083333 2018 T-C2 -8.18 39.64683333 2018 T-C3 -8.18 39.58683333 2018 T-D1 -9.63 39.94633333 2018 T-D2 -9.63 39.848 2018 T-D3 -9.67 39.7635 2018 T-E1 -10.45 40.56933333 2018 T-E2 -10.44 40.67033333 2018 T-E3 -10.44 40.85116667 2018 T-E4 -10.44 41.21533333 2018 T-E5 -10.43 41.7215 2018
